Looking for Migration Genes in the Willow Warbler Genome

“Here today, up and off to somewhere else tomorrow! Travel, change, interest, excitement! The whole world before you, and a horizon that’s always changing!”

– Kenneth Grahame (Wind in the Willows)

 

Migration is one of the most fascinating phenomena in ornithology. How do birds know which way to fly and how do they find their way back? It is well established that migratory behavior has a strong genetic component. Surprisingly, little is known about the exact genes that underlie migration. In principle, you could identify these ‘migration genes’ by comparing the genomes of closely related bird populations that follow different migration routes. And that is exactly what Max Lundberg and his colleagues did.

 

Migratory Divide

In their study, published in Evolution Letters, they focus on two subspecies of the Willow Warbler (Phylloscopus trochilus) in Europe. One subspecies (P. t. trochilus) migrates to the southwest to wintering areas in West Africa, whereas the other subspecies (P. t. acredula) migrates in a southeastern direction to winter in Eastern and Southern Africa. The two populations overlap and interbreed in Sweden giving rise to a particular kind of hybrid zone, a so-called migratory divide (you can read more about this situation here).

 

willow warbler.jpg

A Willow Warbler (from http://www.naturespot.org.uk)

 

A Lot of Data

The researchers performed extensive genetic analyses. They created a de novo assembly of the Willow Warbler genome (i.e. they assembled it from scratch), re-sequenced the whole genomes of nine samples from each population, and designed a molecular marker set (comprised of 6000 Single Nucleotide Polymorphisms or SNPs) for 1152 samples. This impressive dataset revealed that … there was almost no genetic differentiation between the populations. This suggests that these subspecies are at an early stage of divergence.

 

Migration Genes

Nonetheless, three genomic regions – on chromosomes 1, 3 and 5 – were highly differentiated (see the figure below). The genetic markers on chromosome 3 correlated with breeding altitude and latitude, while the regions on chromosomes 1 and 5 perfectly matched the differences in migration route. Zooming in on these regions revealed several genes that are involved in the synthesis of fatty acids.  This seems logical given that long-distance migrants mostly use fat as energy. Furthermore, the subspecies differ significantly in the distance they cover during migration. The authors admit that ‘it is tempting to speculate that these differences represent adaptations in fueling to their different routes.’

willow_warbler_genome

The three differentiated regions (highlighted in red) in the Willow Warbler genome. The remainder of the genome is largely undifferentiated (adapted from Lundberg et al. 2017)

 

References

Lundberg M, Liedvogel M, Larson K, Sigeman H, Grahn M, Wright A, Åkesson S, Bensch S 2017. Genetic differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks. Evolution Letters 1: 155-168.   http://onlinelibrary.wiley.com/doi/10.1002/evl3.15/abstract

 

The paper has been added to the Phylloscopidae page.

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Promiscuous Petrels: Genetic Study Reveals Gene Flow on a Global Scale

A recent study, published in Molecular Ecology, shows inter-oceanic gene flow among five petrel species on a global scale.

Petrels, the narrow-winged seabirds that graciously soar across the world’s oceans, hold a peculiar contradiction. On the one hand, they disperse on a globally exploring distant waters, while, on the other hand, they display a strong instinct to return to their birth place during the breeding season (i.e. natal philopatry). In this respect, they resemble certain scientists who disperse widely, doing postdocs across the globe, only to return to the universities where they obtained their PhDs for a tenure position.

 

trindade petrel

A dark Trindade Petrel (from http://www.hbw.com)

 

Five Species – Three Oceans

How do these contrasting behaviors in petrels translate to their genetics? To explore this question, Katherine Booth Jones and her colleagues sampled no less than 1001 petrels (genus Pterodroma) on a worldwide scale. The sampled birds represented five distinct species, distributed across three oceans (Indian, Atlantic and Pacific):

  • Trindade Petrel (P. arminjoniana)
  • Herald Petrel (P. heraldica)
  • Kerdamec Petrel (P. neglecta)
  • Murphy’s Petrel (P. ultima)
  • Phoenix Petrel (P. alba)

 

Inter-oceanic Gene Flow

Hybridization among petrels is best studied on the Round Island in the Indian Ocean. Here, three species – Trindade, Kerdamec and Herald Petrel – hybridize extensively (read more about this case on the Procellariiformes page). However, the genetic analysis – based on microsatellites – in the present study shows that hybridization is not limited to this island. In fact, gene flow even occurrs between populations from different oceans, in other words: inter-oceanic gene flow.

This results suggests that petrels migrate between oceans. To support this suggestion, the researchers also present tracking data from two individuals that both left the Indian Ocean. One individual traveled eastwards to the Pacific Ocean, whereas another bird explored the Atlantic Ocean in the west.

 

KermadecPetrel

A Kerdamec Petrel (from http://www.hbw.com)

 

Three-way Hybrids

The genetic data also revealed possible hybrids among three different petrel species. In birds, most three-way hybrids are known from captivity (notably falcons), but there is a well-documented case in geese. Dreyen and Gustavsson (2010) report how a hybrid between Swan Goose (Anser cygnoides) and Snow Goose (A. caerulescens) paired up with a Barnacle Goose (Branta leucopsis) and produced offspring. A three-way intergeneric hybrid.

 

Threeway Goose Hybrid

The Swan Goose x Snow Goose hybrid (left) and its offspring with a Barnacle Goose standing on the right (from Dreyen & Gustavsson, 2010)

 

Think big

An important lesson to take away from this petrel study is to think beyond hybrid zones. Most studies focused on narrow contact zones between two species, which has led to important insights into speciation and hybridization. However, I think it is time to expand our view and sample widely to uncover unexpected patterns of gene flow on a global scale.

 

References

Booth Jones K.A., et al. (2017). Widespread gene flow between oceans in a pelagic seabird species complex. Molecular Ecology. 26:5716-5728. https://doi.org/10.1111/mec.14330

Dreyen P. & Gustavsson C. G. (2010). Photographic documentation of a Swan Goose x Snow Goose Anser cygnoides x Anser caerulescens hybrid and its offspring with a Barnacle Goose (Branta leucopsis) – a unique three-species cross. Ornithologischer Anzeiger. 49:41-52.

 

This paper has been added to the Procellariiformes page.

Throwback Thursday: Six Years with a Brewster’s Warbler.

It has been a while since I presented an old Avian Hybrids paper on Thursday. But the next paper, published in 1944 in The Auk, is a gem. It contains six years of observations and no statistics! Sounds like a great read, doesn’t it.

The hybrid in question concerns the so-called Brewster’s Warbler, a cross between Golden-winged (Vermivora chrysoptera) and Blue-winged Warbler (V. pinus). Hybrids between these species were first described as distinct species, namely Lawrence’s Warbler (V. lawrencei) and Brewster’s Warbler (V. leucobronchialis).

Here is the opening paragraph of the paper, written by T. Donald Carter.

In the ‘Auk,’ volume 40, July, 1923, R. H. Howland and I published an account of our discovery of a male Brewster’s Warbler, Vermivora pinus X chrysoptera, mated to a female Golden-winged Warbler, Vermivora chrysoptera. We located his nest and brood and later captured and banded him and three of his young. At the time of the writing we supposed that our story was closed, but it proved to be the first chapter of a six-year acquaintance with this same bird.

The remainder of the paper is a year by year description (running from 1922 to 1927) of the adventures of their Brewster’s Warbler in New Jersey. A fine piece of natural history. I could quote different sections from the paper, but I advice you to read the whole paper. Preferably close to a fire place with a hot beverage.

Click here to read the paper. If you cannot access it, feel free to contact me.

brewsters

The young of a Brewster’s Warbler. Picture taken on June 10, 1922.

References

Carter, T. D. (1944). Six years with a Brewster’s Warbler. The Auk, 48-61.

Becoming Black: The Origins of Melanic Monarcha Flycatchers

Two populations of all black Monarcha Flycatchers might have independent origins.

In 1942, the German ornithologist Ernst Mayr published his seminal book on speciation: Systematics and the Origin of Species: from the Viewpoint of a Zoologist. In this book (which is still a nice read today), he argues that geographic isolation is the main driver of speciation. To support his claims, he discusses the subspecies of the Monarcha castaneiventris flycatcher that resides on the Solomon Islands (located east of Papua New Guinea). In this blogpost, I will focus on two subspecies: megarhynchus and ugiensis.

 

Monarcha distribution

Distribution of the Monarcha castaneiventris subspecies (from: Cooper & Uy 2017)

 

Introducing the Islands

The first subspecies (megarhynchus) is found on the large island of Makira. These birds have chestnut bellies and iridescent blue-back upper parts. The second subspecies (ugiensis) is distributed on nearby satellite islands: Ugi and Three Sisters in the north and Santa Anda and Santa Catalina in the southeast. In contrast to the birds from Makira, this subspecies is entirely blue-black. A recent study in Molecular Ecology provides a genomic perspective on the evolution of this species complex.

monarcha subspecies

Two Monarcha subspecies: the chestnut-bellied megarhynchus and the entirely blue-black ugiensis (from: http://www.hbw.com/)

 

Hybridization or Independent Origins?

Elizabeth Cooper and Albert Uy used over 70,000 genetic markers (SNPs; Single Nucleotide Polymorphisms) to unravel the origin of the blue-black subspecies. Surprisingly, both melanic populations, which Ernst Mayr considered as a single subspecies, do not cluster together. The birds from the southeastern islands are more closely related to the chestnut-bellied individuals from Makira. This pattern can be explained in two ways: hybridization or independent origins.

To solve this riddle, Cooper and Uy performed isolation with migration analyses. The model with the highest likelihood pointed to migration between the large island of Makira and the satellite islands, but not between the satellite islands themselves. This results weakened a role for hybridization. It thus seems that the melanic populations have independent origins. This hypothesis is supported by the observation that different mutations underlie the black plumage color in each population, as shown in a previous study by Albert Uy and colleagues.

From a taxonomic point of view, the melanic populations should be considered separate subspecies. It turns out Ernst Mayr was wrong here. And it’s not the first time he made a mistake. In his 1963 book Animal Species and Evolution, Mayr stated that “the available evidence contradicts the assumption that hybridization plays a major evolutionary role.”

 

References

Cooper, E.A. and J.A.C. Uy, Genomic evidence for convergent evolution of a key trait underlying divergence in island birds. Molecular Ecology, 2017. 26(14): p. 3760-3774.

Mayr, E., Systematics in the origin of species : from the viewpoint of a zoologist. 1942, New York: Harvard University Press.

Mayr, E., Animal species and evolution. 1963, Cambridge: Belknap Press of Harvard University Press. xiv, 797 p.

Uy, J.A.C., et al., Mutations in different pigmentation genes are associated with parallel melanism in island flycatchers. Proceedings of the Royal Society B-Biological Sciences, 2016. 283(1834): p. 20160731.

 

This paper has been added to the Monarchidae page.